Evolution, transitions, and volvocine algae

Volvox, the Fierce Roller, is a model organism for the evolution of multicellularity and cellular differentiation.
I am a biologist who studies the evolution of biological complexity using Volvox and related algae as a study system. I blog about evolutionary biology, astrobiology, philosophy of biology, skepticism, academia and academic publishing, intelligent design and other forms of creationism, and whatever else happens to be on my mind.Read More…

EVENTS

Convergence part 7: convergence in Volvox

Last year I wrote a series of posts on convergent evolution and misrepresentations of the history of the concept by proponents of intelligent design including Günter Bechly, Lee M. Spetner, Granville Sewell, and others. I didn’t intend for there to be a two-month gap before the final installment (nor am I sure this is the final installment), but here we are.

The Discovery Institute is producing a revisionist history. To hear them tell it, convergence is something that evolutionary biologists have either barely heard of or that they “invented” or “made up” to hide problems with the tree of life. Convergence “destroys the tree of life,” it “contradict[s] the [modern synthesis],” and it is “quite unexpected” to evolutionary biologists. All of that is a big, stinking pile of wrong. In reality, biologists since Darwin, and including Darwin, have always appreciated the importance of convergence, have written thousands of papers about it, and have included it in every evolutionary biology textbook I’m aware of.

It’s important to remember that Volvox was one of the first microbes ever described, way back in 1700 by Antonie van Leeuwenhoek himself. Half a century later, Linnaeus gave van Leeuwenhoek’s “great round particles” the name Volvox globator, the spherical fierce roller. Obviously, genetic data weren’t available then, or for a long time afterward, so taxonomy, classification, and inferences about evolutionary relationships among microbes were mainly based on comparisons of the structure and arrangement of cells. As additional species were discovered that looked similar to Volvox globator, they were either named Volvox or assigned to new genera that were assumed to be closely related to Volvox. By the early 20th century, the algae that we today call Volvox had been classified into as many as six different genera. Eventually, these were collapsed into a single genus, Volvox, and the former genera were reduced in taxonomic rank to “sections.”

When molecular sequence data began to trickle in in the early 1990s, the coherence of the genus Volvox began to look shaky right from the start. For example, when Allan Larson, Marilyn Kirk, and David Kirk sequenced ribosomal RNAs from several volvocine species, one species, Volvox capensis, didn’t group with the others:

Figure 5 from Larson et al. 1991. Parsimony tree based on rRNA sequences. Internal nodes are numbered, and the numbers of changes inferred for each branch (including substitutions and length mutations observed at both informative and uninformative sites) are given. Sequences for Chlorella and angiosperms were used as outgroups.

If that tree is right, Volvox is polyphyletic, that is, species assigned to the genus don’t share a unique common ancestor. Any ancestor to all Volvox species is also an ancestor of Eudorina, Pandorina, Platydorina, etc. That could mean one of two things: either all of those genera evolved from a Volvox-like ancestor, or the traits that characterize Volvox evolved at least twice, once in Volvox capensis and once in the ancestor of all other Volvox species.

At this point, we need to have a brief digression about terminology. Taxonomists don’t like taxa to be polyphyletic; in fact, many argue that taxa are only valid if they are monophyletic. Those same people will get mad at me if I continue to refer to “the genus Volvox” while admitting that species so classified may not share a unique common ancestor. I have previously explained why we don’t just give them new names, and I’m not going to get into that here. What I am going to do instead is start referring to them as a “nominal genus,” by which I mean “a group of species that share a genus name,” without any implications for whether or not that name represents a valid genus.

There have been lots and lots of evolutionary trees of volvocine algae published since Larson and colleagues’, and most of them have been based on molecular (RNA or DNA) sequence data. It would take me several long blog posts to go through all of them. Instead, I’m going to skip a couple of decades’-worth of hard work by several lab groups and simply say that the situation hasn’t improved. The more we learn about volvocine relationships, the less likely it seems that the nominal genus Volvox is monophyletic.

Rather, there seem to be three, or possibly even four, separate evolutionary lineages that have converged on the characters we think of as characteristic of Volvox:

The figure above is a fair summary of the current consensus view of evolutionary relationships among volvocine algae. Just as in the Larson tree, there is no ancestor of all Volvox species that isn’t also ancestral to other genera. The monophyletic groups (clades) comprised of Volvox species are (from top to bottom) Volvox aureus, the group from Volvox carteri through Volvox africanus, Volvox gigas, and the group made up of Volvox globator and Volvox barberi. For reasons of parsimony (that is, a smaller number of required changes), we think that at least three of these groups evolved the Volvox suite of characters independently. Volvox aureus might represent a fourth origin, or it might be that the ancestor of Volvox aureus and Volvox carteri through africanus was Volvox-like, and that Pleodorina californica lost some of those characters.

These inferences are, of course, dependent on the tree being right, or at least mostly right. There is an entire subfield of evolutionary biology, with several dedicated journals and many thousands of publications, devoted to figuring out the best ways to infer evolutionary relationships. The massive volume of literature this subfield has produced can be summed up as “it’s not that easy.” There are lots of reasons an inferred evolutionary tree can be wrong, and given the massive numbers of possible trees (on the order of 1027 for the taxa in the tree above), it’s nearly certain that any large tree is wrong in at least a few details.

For Volvox to be monophyletic, though, nearly all of the phylogenetic trees inferred in the last couple of decades would have to be wrong, not just in the details but badly wrong in terms of the backbone relationships. Furthermore, there are reasons independent of molecular sequence data to think that Volvox is polyphyletic, for example important differences in developmental programs and in colony structure. So unless our understanding of volvocine evolution is badly wrong, several traits characteristic of Volvox have evolved multiple times in independently evolving lineages: colonies with several hundred to tens of thousands of small somatic cells, much smaller numbers of reproductive cells, and oogamy (eggs and sperm) in sexual reproduction.

Is that really so surprising, though? There’s reason to think that all three of those traits are related to one thing: size. Large colonies need lots of somatic cells, because it’s the flagella of the somatic cells that provide propulsion, and it takes more propulsion to move a large colony than a small one. Physical constraints prevent large colonies from having large numbers of reproductive cells, since those reproductive cells need to be big. Cells are denser than water, so too many big reproductive cells makes it hard to swim (Cristian Solari and colleagues have modeled both of these factors). Finally, oogamy seems to be a nearly inevitable consequence of large body size, as nearly every multicellular group has evolved sperm and eggs. There is a good bit of theory to explain why this is the case, which I won’t get into here, but Erik Hanschen and colleagues have provided comparative evidence that it is size per se that drove the evolution of oogamy in Volvox (full disclosure: I’m a junior author).

But that still leaves the question of why large size would have evolved more than once (large is relative here, perhaps 1/4 to 3 mm). On this question, I can only speculate. What we do know is that body size is something that changes often and relatively rapidly in evolutionary terms (it is evolutionarily labile, in other words). We also know that volvocine habitats, which are mostly lakes and ponds, are discontinuous and often very isolated. If dispersal among ponds is infrequent, it’s possible that multiple lineages increased in size simply because some members of those lineages found themselves isolated in habitats in which increased size was advantageous.

Like many other examples of convergence, the fact that apparently very similar species are not, in fact, close relatives, seems surprising. It’s not so surprising, though, that we don’t have a plausible explanation. Of course, we can’t know the exact sequence of dispersal events, mutations, and selective pressures that led to three independent lineages convergently evolving a similar set of traits. It becomes a lot less surprising, though, when we consider that those traits may be linked, either functionally or genetically, so that the evolution of one is likely to lead to the evolution of all. If, as John Tyler Bonner has often suggested, the driver of all of this is size, it’s not at all surprising that increased size is adaptive in some habitats.

And that is the take-home message of this series. Convergent evolution is exactly what we should expect to see if similar habitats or lifestyles impose similar selective pressures. A lifestyle of jumping from tree to tree has often driven the evolution of flaps of skin that allow some degree of gliding. A lifestyle of rapid swimming has often driven the evolution of a fusiform body. A nocturnal lifestyle has often driven the evolution of big eyes, and a complete lack of light has often driven their reduction or loss. Convergent evolution is not contrary to anything in evolutionary theory; it is, in fact, part of what led Charles Darwin to conceive his theory of evolution by natural selection.

Nor is convergent evolution evidence against common descent. When intelligent design proponents like Cornelius Hunter express their incredulity that two distantly related species could have evolved a similar appearance, they are only telling half of the story. Yes, some traits of these species are remarkably similar: in the sugar glider and flying squirrel example, both nocturnal forest dwellers have evolved large eyes and a way to move from tree to tree without coming down to the ground. But each shares many more traits with the other members of its own taxonomic order, just as we would expect if each order descended from a different ancestor:

…one is a marsupial and one a placental mammal, and as expected they have significant differences in their reproductive systems, structure of the skull and brain, dental formulas, length of gestation, and other traits. Differences, that is, that they share with other marsupials and placentals, respectively.

Focusing only on the traits that are shared between distantly related species, and ignoring the much larger number of traits that differ, is an example of cherry picking. Pretending that evolutionary biologists have only recently discovered convergence is an example of historical revisionism. There’s no way to know which of these arguments stem from ignorance and which from dishonesty. But we do know that they’re wrong.